IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39220-y.html
   My bibliography  Save this article

Structure and proposed DNA delivery mechanism of a marine roseophage

Author

Listed:
  • Yang Huang

    (Xiamen University
    Xiamen University)

  • Hui Sun

    (Xiamen University
    Xiamen University)

  • Shuzhen Wei

    (Xiamen University)

  • Lanlan Cai

    (The Hong Kong University of Science and Technology)

  • Liqin Liu

    (Xiamen University
    Xiamen University)

  • Yanan Jiang

    (Xiamen University
    Xiamen University)

  • Jiabao Xin

    (Xiamen University
    Xiamen University)

  • Zhenqin Chen

    (Xiamen University
    Xiamen University)

  • Yuqiong Que

    (Xiamen University
    Xiamen University)

  • Zhibo Kong

    (Xiamen University
    Xiamen University)

  • Tingting Li

    (Xiamen University
    Xiamen University)

  • Hai Yu

    (Xiamen University
    Xiamen University)

  • Jun Zhang

    (Xiamen University
    Xiamen University)

  • Ying Gu

    (Xiamen University
    Xiamen University)

  • Qingbing Zheng

    (Xiamen University
    Xiamen University)

  • Shaowei Li

    (Xiamen University
    Xiamen University)

  • Rui Zhang

    (Xiamen University
    Shenzhen University)

  • Ningshao Xia

    (Xiamen University
    Xiamen University
    Chinese Academy of Medical Sciences)

Abstract

Tailed bacteriophages (order, Caudovirales) account for the majority of all phages. However, the long flexible tail of siphophages hinders comprehensive investigation of the mechanism of viral gene delivery. Here, we report the atomic capsid and in-situ structures of the tail machine of the marine siphophage, vB_DshS-R4C (R4C), which infects Roseobacter. The R4C virion, comprising 12 distinct structural protein components, has a unique five-fold vertex of the icosahedral capsid that allows genome delivery. The specific position and interaction pattern of the tail tube proteins determine the atypical long rigid tail of R4C, and further provide negative charge distribution within the tail tube. A ratchet mechanism assists in DNA transmission, which is initiated by an absorption device that structurally resembles the phage-like particle, RcGTA. Overall, these results provide in-depth knowledge into the intact structure and underlining DNA delivery mechanism for the ecologically important siphophages.

Suggested Citation

  • Yang Huang & Hui Sun & Shuzhen Wei & Lanlan Cai & Liqin Liu & Yanan Jiang & Jiabao Xin & Zhenqin Chen & Yuqiong Que & Zhibo Kong & Tingting Li & Hai Yu & Jun Zhang & Ying Gu & Qingbing Zheng & Shaowei, 2023. "Structure and proposed DNA delivery mechanism of a marine roseophage," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39220-y
    DOI: 10.1038/s41467-023-39220-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39220-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39220-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lei Sun & Xinzheng Zhang & Song Gao & Prashant A. Rao & Victor Padilla-Sanchez & Zhenguo Chen & Siyang Sun & Ye Xiang & Sriram Subramaniam & Venigalla B. Rao & Michael G. Rossmann, 2015. "Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    2. Jed A. Fuhrman, 1999. "Marine viruses and their biogeochemical and ecological effects," Nature, Nature, vol. 399(6736), pages 541-548, June.
    3. Pavol Bárdy & Tibor Füzik & Dominik Hrebík & Roman Pantůček & J. Thomas Beatty & Pavel Plevka, 2020. "Structure and mechanism of DNA delivery of a gene transfer agent," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Nicholas P. Stone & Gabriel Demo & Emily Agnello & Brian A. Kelch, 2019. "Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    5. Yun-Tao Liu & Jonathan Jih & Xinghong Dai & Guo-Qiang Bi & Z. Hong Zhou, 2019. "Cryo-EM structures of herpes simplex virus type 1 portal vertex and packaged genome," Nature, Nature, vol. 570(7760), pages 257-261, June.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Natalia Quinones-Olvera & Siân V. Owen & Lucy M. McCully & Maximillian G. Marin & Eleanor A. Rand & Alice C. Fan & Oluremi J. Martins Dosumu & Kay Paul & Cleotilde E. Sanchez Castaño & Rachel Petherbr, 2024. "Diverse and abundant phages exploit conjugative plasmids," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xudong Jia & Yuanzhu Gao & Yuxuan Huang & Linjun Sun & Siduo Li & Hongmei Li & Xueqing Zhang & Yinyin Li & Jian He & Wenbi Wu & Harikanth Venkannagari & Kai Yang & Matthew L. Baker & Qinfen Zhang, 2023. "Architecture of the baculovirus nucleocapsid revealed by cryo-EM," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Fenglin Li & Chun-Feng David Hou & Ravi K. Lokareddy & Ruoyu Yang & Francesca Forti & Federica Briani & Gino Cingolani, 2023. "High-resolution cryo-EM structure of the Pseudomonas bacteriophage E217," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Igor Orlov & Stéphane Roche & Sandrine Brasilès & Natalya Lukoyanova & Marie-Christine Vaney & Paulo Tavares & Elena V. Orlova, 2022. "CryoEM structure and assembly mechanism of a bacterial virus genome gatekeeper," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Keller, David P. & Hood, Raleigh R., 2011. "Modeling the seasonal autochthonous sources of dissolved organic carbon and nitrogen in the upper Chesapeake Bay," Ecological Modelling, Elsevier, vol. 222(5), pages 1139-1162.
    5. Yuanmin Sun & Kunxian Tang & Hui Song & Degang Jiang & Shan Chen & Wulin Tu & Luchun Cai & Haiping Huang & Fei Zhang, 2022. "The Effect of Domestic Sewage Treatment on Islands Using Ecological Treatment Processes: A Case Study of Haimen Island, Fujian Province," IJERPH, MDPI, vol. 19(23), pages 1-12, November.
    6. Yuxuan Du & Jed A. Fuhrman & Fengzhu Sun, 2023. "ViralCC retrieves complete viral genomes and virus-host pairs from metagenomic Hi-C data," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Krishna, Shubham & Peterson, Victoria & Listmann, Luisa & Hinners, Jana, 2024. "Interactive effects of viral lysis and warming in a coastal ocean identified from an idealized ecosystem model," Ecological Modelling, Elsevier, vol. 487(C).
    8. Xiaomei Feng & Yuan Miao & Shulin Sun & Lei Wang, 2022. "Dynamic Behaviors of a Stochastic Eco-Epidemiological Model for Viral Infection in the Toxin-Producing Phytoplankton and Zooplankton System," Mathematics, MDPI, vol. 10(8), pages 1-18, April.
    9. Sun, Zhe & Zhou, Zhi, 2019. "Nature-inspired virus-assisted algal cell disruption for cost-effective biofuel production," Applied Energy, Elsevier, vol. 251(C), pages 1-1.
    10. Stephen J. Beckett & David Demory & Ashley R. Coenen & John R. Casey & Mathilde Dugenne & Christopher L. Follett & Paige Connell & Michael C. G. Carlson & Sarah K. Hu & Samuel T. Wilson & Daniel Murat, 2024. "Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    11. Guosong Wang & Zhenghui Zha & Pengfei Huang & Hui Sun & Yang Huang & Maozhou He & Tian Chen & Lina Lin & Zhenqin Chen & Zhibo Kong & Yuqiong Que & Tingting Li & Ying Gu & Hai Yu & Jun Zhang & Qingbing, 2022. "Structures of pseudorabies virus capsids," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    12. Zhihai Li & Jingjing Pang & Rongchao Gao & Qingxia Wang & Maoyan Zhang & Xuekui Yu, 2023. "Cryo-electron microscopy structures of capsids and in situ portals of DNA-devoid capsids of human cytomegalovirus," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    13. Yantao Liang & Li Li & Tingwei Luo & Yao Zhang & Rui Zhang & Nianzhi Jiao, 2014. "Horizontal and Vertical Distribution of Marine Virioplankton: A Basin Scale Investigation Based on a Global Cruise," PLOS ONE, Public Library of Science, vol. 9(11), pages 1-11, November.
    14. Jun-Tao Zhang & Xiao-Yu Liu & Zhuolin Li & Xin-Yang Wei & Xin-Yi Song & Ning Cui & Jirui Zhong & Hongchun Li & Ning Jia, 2024. "Structural basis for phage-mediated activation and repression of bacterial DSR2 anti-phage defense system," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Smeti, Evangelia & Roelke, Daniel L. & Tsirtsis, George & Spatharis, Sofie, 2018. "Species extinctions strengthen the relationship between biodiversity and resource use efficiency," Ecological Modelling, Elsevier, vol. 384(C), pages 75-86.
    16. Jingen Zhu & Himanshu Batra & Neeti Ananthaswamy & Marthandan Mahalingam & Pan Tao & Xiaorong Wu & Wenzheng Guo & Andrei Fokine & Venigalla B. Rao, 2023. "Design of bacteriophage T4-based artificial viral vectors for human genome remodeling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Christian Winter & Jérôme P Payet & Curtis A Suttle, 2012. "Modeling the Winter–to–Summer Transition of Prokaryotic and Viral Abundance in the Arctic Ocean," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39220-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.